Transcranial brain stimulation to promote functional recovery after stroke

Purpose of review Noninvasive brain stimulation (NIBS) is increasingly used to enhance the recovery of function after stroke. The purpose of this review is to highlight and discuss some unresolved questions that need to be addressed to better understand and exploit the potential of NIBS as a therapeutic tool. Recent findings Recent meta-analyses showed that the treatment effects of NIBS in patients with stroke are rather inconsistent across studies and the evidence for therapeutic efficacy is still uncertain. This raises the question of how NIBS can be developed further to improve its therapeutic efficacy. Summary This review addressed six questions: How does NIBS facilitate the recovery of function after stroke? Which brain regions should be targeted by NIBS? Is there a particularly effective NIBS modality that should be used? Does the location of the stroke influence the therapeutic response? How often should NIBS be repeated? Is the functional state of the brain during or before NIBS relevant to therapeutic efficacy of NIBS? We argue that these questions need to be tackled to obtain sufficient mechanistic understanding of how NIBS facilitates the recovery of function. This knowledge will be critical to fully unfold the therapeutic effects of NIBS and will pave the way towards adaptive NIBS protocols, in which NIBS is tailored to the individual patient.

[1]  Sergio P. Rigonatti,et al.  Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. , 2007, Restorative neurology and neuroscience.

[2]  Jean-Louis Thonnard,et al.  Single Session of Dual-tDCS Transiently Improves Precision Grip and Dexterity of the Paretic Hand After Stroke , 2014, Neurorehabilitation and neural repair.

[3]  Á. Pascual-Leone,et al.  Modulation of spinal cord excitability by subthreshold repetitive transcranial magnetic stimulation of the primary motor cortex in humans , 2001, Neuroreport.

[4]  Hannah J. Block,et al.  Can cerebellar transcranial direct current stimulation become a valuable neurorehabilitation intervention? , 2012, Expert review of neurotherapeutics.

[5]  W. Byblow,et al.  Combining Theta Burst Stimulation With Training After Subcortical Stroke , 2010, Stroke.

[6]  Felipe Fregni,et al.  Classification of methods in transcranial Electrical Stimulation (tES) and evolving strategy from historical approaches to contemporary innovations , 2013, Journal of Neuroscience Methods.

[7]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[8]  Christian Gerloff,et al.  Modulation of Training by Single-Session Transcranial Direct Current Stimulation to the Intact Motor Cortex Enhances Motor Skill Acquisition of the Paretic Hand , 2012, Stroke.

[9]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[10]  Markus Zahn,et al.  Transcranial magnetic stimulation and stroke: A computer-based human model study , 2006, NeuroImage.

[11]  S. Arndt,et al.  Repetitive transcranial magnetic stimulation as treatment of poststroke depression: a preliminary study , 2004, Biological Psychiatry.

[12]  R. Nudo,et al.  Motor and Premotor Cortices in Subcortical Stroke , 2013, Neurorehabilitation and neural repair.

[13]  V Achache,et al.  Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects , 2011, The Journal of physiology.

[14]  M. Linsdell,et al.  One hertz repetitive transcranial magnetic stimulation over dorsal premotor cortex enhances offline motor memory consolidation for sequence‐specific implicit learning , 2013, The European journal of neuroscience.

[15]  Gary W. Thickbroom,et al.  Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models , 2007, Experimental Brain Research.

[16]  Bernhard Elsner,et al.  Transcranial direct current stimulation (tDCS) for improving aphasia in patients after stroke. , 2013, The Cochrane database of systematic reviews.

[17]  Gereon R. Fink,et al.  Disruption of motor network connectivity post-stroke and its noninvasive neuromodulation. , 2012, Current opinion in neurology.

[18]  M. Donohue,et al.  rTMS for suppressing neuropathic pain: a meta-analysis. , 2009, The journal of pain : official journal of the American Pain Society.

[19]  Giulio Ruffini,et al.  The electric field in the cortex during transcranial current stimulation , 2013, NeuroImage.

[20]  Heidi Johansen-Berg,et al.  Predicting behavioural response to TDCS in chronic motor stroke☆ , 2014, NeuroImage.

[21]  Ethan R. Buch,et al.  Noninvasive brain stimulation: from physiology to network dynamics and back , 2013, Nature Neuroscience.

[22]  R. Ricci,et al.  Behavioral and neuroplastic effects of low-frequency rTMS of the unaffected hemisphere in a chronic stroke patient: A concomitant TMS and fMRI study , 2014, Neurocase.

[23]  Alexander Opitz,et al.  Impact of the gyral geometry on the electric field induced by transcranial magnetic stimulation , 2011, NeuroImage.

[24]  M. Hallett,et al.  Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior , 2000, Clinical Neurophysiology.

[25]  Jeffrey S. Johnson,et al.  Using EEG to Explore How rTMS Produces Its Effects on Behavior , 2009, Brain Topography.

[26]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[27]  Min Ho Chun,et al.  Effect of high- and low-frequency repetitive transcranial magnetic stimulation on visuospatial neglect in patients with acute stroke: a double-blind, sham-controlled trial. , 2013, Archives of physical medicine and rehabilitation.

[28]  A. Thiel,et al.  Effects of Noninvasive Brain Stimulation on Language Networks and Recovery in Early Poststroke Aphasia , 2013, Stroke.

[29]  G. Tononi,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Repetitive Transcranial Magnetic Stimulation Affects Behavior by Biasing Endogenous Cortical Oscillations , 2022 .

[30]  J. Szaflarski,et al.  Changes in white matter integrity follow excitatory rTMS treatment of post-stroke aphasia. , 2012, Restorative neurology and neuroscience.

[31]  Geraint Rees,et al.  Stochastic Resonance Effects Reveal the Neural Mechanisms of Transcranial Magnetic Stimulation , 2011, The Journal of Neuroscience.

[32]  J. Liepert,et al.  Improvement of dexterity by single session low-frequency repetitive transcranial magnetic stimulation over the contralesional motor cortex in acute stroke: a double-blind placebo-controlled crossover trial. , 2007, Restorative neurology and neuroscience.

[33]  J. Rothwell,et al.  Effect of Anodal Versus Cathodal Transcranial Direct Current Stimulation on Stroke Rehabilitation , 2013, Neurorehabilitation and neural repair.

[34]  Ming Liu,et al.  Repetitive transcranial magnetic stimulation for improving function after stroke. , 2013, The Cochrane database of systematic reviews.

[35]  Nicole Wenderoth,et al.  Task-Specific Effect of Transcranial Direct Current Stimulation on Motor Learning , 2013, Front. Hum. Neurosci..

[36]  Alexander Münchau,et al.  Shaping the excitability of human motor cortex with premotor rTMS , 2004, The Journal of physiology.

[37]  Mark D. McDonnell,et al.  The benefits of noise in neural systems: bridging theory and experiment , 2011, Nature Reviews Neuroscience.

[38]  R. Hanajima,et al.  Bidirectional long‐term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation , 2008, The Journal of physiology.

[39]  M. Urashima,et al.  A multi-center study on low-frequency rTMS combined with intensive occupational therapy for upper limb hemiparesis in post-stroke patients , 2012, Journal of NeuroEngineering and Rehabilitation.

[40]  H. Tsang,et al.  A review on the effectiveness of repetitive transcranial magnetic stimulation (rTMS) on post-stroke aphasia , 2013, Reviews in the neurosciences.

[41]  Alexander Münchau,et al.  Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans , 2008, The European journal of neuroscience.

[42]  Heidi Johansen-Berg,et al.  Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke , 2011, Brain : a journal of neurology.

[43]  M. Bove,et al.  Associative cortico-cortical plasticity may affect ipsilateral finger opposition movements , 2011, Behavioural Brain Research.

[44]  J. Rothwell,et al.  Level of action of cathodal DC polarisation induced inhibition of the human motor cortex , 2003, Clinical Neurophysiology.

[45]  F. Chollet,et al.  Neural substrates of low‐frequency repetitive transcranial magnetic stimulation during movement in healthy subjects and acute stroke patients. A PET study , 2009, Human brain mapping.

[46]  Sergio P. Rigonatti,et al.  A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients , 2005, Neurology.

[47]  C. Caltagirone,et al.  Theta-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect , 2012, Neurology.

[48]  Christian Gerloff,et al.  The Role of Multiple Contralesional Motor Areas for Complex Hand Movements after Internal Capsular Lesion , 2006, The Journal of Neuroscience.

[49]  D. Krieger Therapeutic drug approach to stimulate clinical recovery after brain injury. , 2013, Frontiers of neurology and neuroscience.

[50]  F. Fregni,et al.  Systematic Review of Parameters of Stimulation, Clinical Trial Design Characteristics, and Motor Outcomes in Non-Invasive Brain Stimulation in Stroke , 2012, Front. Psychiatry.

[51]  H. Benali,et al.  Contribution of Corticospinal Tract and Functional Connectivity in Hand Motor Impairment after Stroke , 2013, PloS one.

[52]  Sergio P. Rigonatti,et al.  Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory , 2005, Experimental Brain Research.

[53]  H. Siebner,et al.  Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex , 2005, Experimental Brain Research.

[54]  C. Pecoraro,et al.  Modulatory effects of 1 Hz rTMS over the cerebellum on motor cortex excitability , 2006, Experimental Brain Research.

[55]  Yoshikazu Ugawa,et al.  State-Dependent and Timing-Dependent Bidirectional Associative Plasticity in the Human SMA-M1 Network , 2011, The Journal of Neuroscience.

[56]  Á. Pascual-Leone,et al.  A Review of Combined TMS-EEG Studies to Characterize Lasting Effects of Repetitive TMS and Assess Their Usefulness in Cognitive and Clinical Neuroscience , 2009, Brain Topography.

[57]  M. Nitsche,et al.  The pharmacology of neuroplasticity induced by non‐invasive brain stimulation: building models for the clinical use of CNS active drugs , 2012, The Journal of physiology.

[58]  Antonio Oliviero,et al.  The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence , 2002, Clinical Neurophysiology.

[59]  Gereon R. Fink,et al.  Interhemispheric Competition After Stroke: Brain Stimulation to Enhance Recovery of Function of the Affected Hand , 2009, Neurorehabilitation and neural repair.

[60]  Alexander Münchau,et al.  Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans , 2003, NeuroImage.

[61]  Simon B. Eickhoff,et al.  Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling , 2010, NeuroImage.

[62]  W. Kakuda,et al.  Combination Treatment of Low-Frequency rTMS and Occupational Therapy with Levodopa Administration: An Intensive Neurorehabilitative Approach for Upper Limb Hemiparesis After Stroke , 2011, The International journal of neuroscience.

[63]  S. Riek,et al.  Long term language recovery subsequent to low frequency rTMS in chronic non-fluent aphasia. , 2013, NeuroRehabilitation.

[64]  J. Schwarzbach,et al.  State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices. , 2010, Cerebral cortex.

[65]  J. Rothwell,et al.  Consensus: Motor cortex plasticity protocols , 2008, Brain Stimulation.

[66]  G. Deuschl,et al.  Inducing homeostatic-like plasticity in human motor cortex through converging corticocortical inputs. , 2009, Journal of neurophysiology.

[67]  L. Cohen,et al.  Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. , 2005, Brain : a journal of neurology.

[68]  P. Rossini,et al.  Consensus paper: Combining transcranial stimulation with neuroimaging , 2009, Brain Stimulation.

[69]  F. Barone,et al.  Pharmacologic Interventions for Stroke: Looking Beyond the Thrombolysis Time Window Into the Penumbra With Biomarkers, Not a Stopwatch , 2009, Stroke.

[70]  L. Boyd,et al.  Excitatory repetitive transcranial magnetic stimulation to left dorsal premotor cortex enhances motor consolidation of new skills , 2009, BMC Neuroscience.

[71]  Christian Grefkes,et al.  Differential effects of high‐frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke , 2009, Annals of neurology.

[72]  J. Rothwell,et al.  Preconditioning of Low-Frequency Repetitive Transcranial Magnetic Stimulation with Transcranial Direct Current Stimulation: Evidence for Homeostatic Plasticity in the Human Motor Cortex , 2004, The Journal of Neuroscience.

[73]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

[74]  J. C. Rothwell,et al.  Exploring Theta Burst Stimulation as an intervention to improve motor recovery in chronic stroke , 2007, Clinical Neurophysiology.

[75]  A. Butler,et al.  A meta-analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors. , 2013, Journal of hand therapy : official journal of the American Society of Hand Therapists.

[76]  Kuan-Lin Lai,et al.  rTMS Combined With Task-Oriented Training to Improve Symmetry of Interhemispheric Corticomotor Excitability and Gait Performance After Stroke , 2012, Neurorehabilitation and neural repair.

[77]  Janine Reis,et al.  Modulation of motor performance and motor learning by transcranial direct current stimulation. , 2011, Current opinion in neurology.